The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility

Molecular Cell

Volumn 5, Issue 1, 2000, Pages 73-83

  Yuan, Li ^a   Liu, Jian Guo ^a   Zhao, Jian ^a   Brundell, Eva ^a   Daneholt, Bertil ^a   Höög, Christer ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

RECOMBINANT PROTEIN;

APOPTOSIS; ARTICLE; CELL DEATH; CHROMOSOME; CHROMOSOME PAIRING; DNA REPAIR; FEMALE; GENE; GENE FUNCTION; MALE; MALE FERTILITY; MEIOSIS; MOUSE; MUTATION; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN STRUCTURE;

MURINAE;

EID: 0033975302     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(00)80404-9     Document Type: Article

References (50)

1. Ashley, T., Plug, A.W., Xu, J., Solari, A.J., Reddy, G., Golub, E.I., and Ward, D.C. (1995). Dynamic changes in Rad51 distribution on chromatin in male and female vertebrates. Chromosoma 704,19-28.
2. Bailis, J.M., and Roeder, G.S. (1998). Synaptonemal complex morphogenesis and sister-chromatid cohesion require Mek1-dependent phosphorylation of a meiotic chromosomal protein. Genes Dev. 12, 3551-3563.
3. Barlow, A.L., Benson, F.E., West, S.C., and Hulten, M.A. (1997a). Distribution of the Rad51 recombinase in human and mouse spermatocytes. EMBO J. 16, 5207-5215.
4. Barlow, C., Liyanage, M., Moens, P.B., Deng, C.-X., Ried, T., and Wynshaw-Boris, A. (1997b). Partial rescue of the prophase I defects of Atm-deficient mice by p53 and p21 null alleles. Nat. Genet. 17, 462-466.
5. Barlow, C., Liyanage, M., Moens, P.B., Tarsounas, M., Nagashima, K., Brown, K., Rottinghaus, S., Jackson, S.P., Tagle, D., Ried, T., and Wynshaw-Boris, A. (1998). Atm deficiency results in severe meiotic disruption as early as leptonema of prophase I. Development 125, 4007-4017.
6. Bellvé, A.R., Cavicchia, J.C., Millette, C.F., O'Brien, D.A., Bhatnagar, Y.M., and Dym, M. (1977). Spermatogenic cells of the prepubertal mouse: isolation and morphological characterization. J. Cell Biol. 74, 68-85.
7. Bickel, S.E., and Orr-Weaver, T.L. (1996). Holding chromatids together to ensure they go their separate ways. Bioessays 18, 293-300.
8. Carpenter, A.T.C. (1987). Gene conversion, recombination nodules, and the initiation of meiotic synapsis. Bioessays 6, 232-236.
9. de Vries, S.S., Baart, E.B., Dekker, M., Siezen, A., de Rooij, D.G., de Boer, P., and te Riele, H. (1999). Mouse MutS-like protein Msh5 is required for proper chromosome synapsis in male and female meiosis. Genes Dev. 13, 523-531.
10. Dobson, M.J., Pearlman, R.E., Karaiskakis, A., Spyropoulos, B., and Moens, P.B. (1994). Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J. Cell Sci. 107, 2749-2760.
11. Dresser, M.E., and Moses, M.J. (1979). Silver staining of synaptonemal complexes in surface spreads for light and electron microscopy. Exp. Cell. Res. 121, 416-419.
12. Edelmann, W., Cohen, P.E., Kneitz, B., Winand, N., Lia, M., Heyer, J., Kolodner, R., Pollard, J.W., and Kucherlapati, R. (1999). Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat. Genet. 21, 123-127.
13. Fawcett, D.W. (1956). The fine structure of chromosomes in the meiotic prophase of vertebrate spermatocytes. J. Biophys. Biochem. Cytol. 2, 403-406.
14. Heyting, C. (1996). Synaptonemal complexes: structure and function. Curr. Opin. Cell Biol. 8, 389-396.
15. Kleckner, N. (1996). Meiosis: how could it work? Proc. Natl. Acad. Sci. USA 93, 8167-8174.
16. Klein, F., Mahr, P., Galova, M., Buonomo, S.B.C., Michaelis, C., Nairz, K., and Nasmyth, K. (1999). A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98, 91-103.
17. Krege, J.H., John, S.W., Langenbach, L.L., Hodgin, J.B., Hagaman, J.R., Bachman, E.S., Jennete, J.C., O'Brien, D.A., and Smithies, O. (1995). Male-female differences in fertility and blood pressure in ACE-deficient mice. Nature 375, 146-148.
18. Lammers, J.H.M., Offenberg, H.H., van Aalderen, M., Vink, A.C.G., Dietrich, A.J.J., and Heyting, C. (1994). The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol. Cell. Biol. 14, 1137-1146.
19. Liu, J.G., Yuan, L., Brundell, E., Björkroth, B., Daneholt, B., and Höög, C. (1996). Localization of the N-terminus of SCP1 to the central element of the synaptonemal complex and evidence for direct interactions between the N-termini of SCP1 molecules organized head-to-head. Exp. Cell Res. 226, 11-19.
20. Liu, D., Matzuk, M.M., Sung, W.K., Guo, Q., Wang, P., and Wolgemuth, D.J. (1998). Cyclin A1 is required for meiosis in the male mouse. Nat. Genet. 20, 377-380.
21. Meuwissen, R.L.J., Offenberg, H.H., Dietrich, A.J.J., Riesewijk, A., van lersel, M., and Heyting, C. (1992). A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J. 11, 5091-5100.
22. Miyazaki, W.Y., and Orr-Weaver, T.L. (1994). Sister-chromatid cohesion in mitosis and meiosis. Annu. Rev. Genet. 28, 167-187.
23. Moens, P.B., and Pearlmann, R.E. (1988). Chromatin organization at meiosis. Bioessays 9, 151-153.
24. Moens, P.B., and Spyropoulos, B. (1995). Immunocytology of chiasmata and chromosomal disjunction at mouse meiosis. Chromosoma 104, 175-183.
25. Moses, M.J. (1956). Chromosomal structures in crayfish spermatocytes. J. Biophys. Biochem. Cytol. 2, 215-218.
26. Nasmyth, K. (1999). Separating sister chromatids. Trends Biochem. Sci. 24, 98-104.
27. Offenberg, H.H., Schalk, J.A.C., Meuwissen, R.L.J., van Aalderen, M., Kester, H.A., Dietrich, A.J.J., and Heyting, C. (1998). SCP2: a major protein component of the axial elements of synaptonemal complexes of the rat. Nucleic Acids Res. 26, 2572-2579.
28. Peters, A.H.F.M., Plug, A.W., van Vugt, M.J., and de Boer, P. (1997). A drying-down technique for spreading of mammalian meiocyes from the male and the female germ line. Chromosome Res. 5, 66-71.
29. Pittman, D.L., Cobb, J., Schimenti, K.J., Wilson, L.A., Cooper, D.M., Brignull, E., Handel, M.A., and Schimenti, J.C. (1998). Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol. Cell 1, 697-705.
30. Plug, A.W., Peters, A.H.F.M., Xu, Y., Keegan, K.S., Hoekstra, M.F., Baltimore, D., de Boer, P., and Ashley, T. (1997). ATM and RPA in meiotic chromosome synapsis and recombination. Nat. Genet. 17, 457-461.
31. Plug, A.W., Peters, A.H.F., Keegan, K.S., Hoekstra, M.F., de Boer, P., and Ashley, T. (1998). Changes in protein composition of meiotic nodules during mammalian meiosis. J. Cell Sci. 111, 413-423.
32. Roeder, G.S. (1997). Meiotic chromosomes: it takes two to tango. Genes Dev. 11, 2600-2621.
33. Russel, L.D., Ettlin, R.A., Hakim, A.P.S., and Clegg, E.D. (1990). Histological and Histopathological Evaluation of the Testis (Clearwater, FL: Cache River Press).
34. Schalk, J.A.C., Dietrich, A.J.J., Vink, A.C.G., Offenberg, H.H., van Aalderen, M., and Heyting, C. (1998). Localization of SCP2 and SCP3 protein molecules within synaptonemal complexes of the rat. Chromosoma 107, 540-548.
35. Scherthan, H., Weich, S., Schwegler, H., Heyting, C., Härle, M., and Cremer, T. (1996). Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J. Cell Biol. 134, 1109-1125.
36. Schmekel, K., and Daneholt, B. (1995). The central region of the synaptonemal complex revealed in three dimensions. Trends Biol. Sci. 5, 239-242.
37. Schmekel, K., Meuwissen, R.L.J., Dietrich, A.J.J., Vink, A.C.G., van Marie, H., and Heyting, C. (1996). Organization of SCP1 protein molecules within synaptonemal complexes of rats. Exp. Cell Res. 226, 20-30.
38. Smith, A.V., and Roeder, G.S. (1997). The yeast Red1 protein localizes to the cores of meiotic chromosomes. J. Cell Biol. 136, 957-967.
39. Sym, M., and Roeder, G.S. (1994). Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79, 283-292.
40. Sym, M., and Roeder, G.S. (1995). Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J. Cell Biol. 128, 455-466.
41. Tarsounas, M., Pearlman, R.E., Gasser, P.J., Park, M.S., and Moens, P.B. (1997). Protein-protein interactions in the synaptonemal complex. Mol. Biol. Cell 8, 1405-1414.
42. Toscani, A., Mettus, R.V., Coupland, R., Simpins, H., Litvin, J., Orth, J., Hatton, K.S., and Reddy, E.P. (1997). Arrest of spermatogenesis and defective breast development in mice lacking A-myb. Nature 386, 713-717.
43. von Wettstein, D., Rasmussen, S.W., and Holm, P.B. (1984). The synaptonemal complex and genetic segregation. Annu. Rev. Genet. 18, 331-413.
44. Watanabe, Y., and Nurse, P. (1999). Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400, 461-464.
45. Xu, Y., Ashley, T., Brainerd, E.E., Bronson, R.T., Meyn, M.S., and Baltimore, D. (1996). Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 10, 2411-2422.
46. Yagi, T., Nada, S., Watanabe, N., Tamemoto, H., Kohmura, N., Ikawa, Y., and Aizawa, S. (1993). A novel negative selection for homologous recombinants using diphtheria toxin A fragment gene. Anal. Biochem. 214, 77-86.
47. Yoshida, K., Kondoh, G., Matsuda, Y., Habu, T., Nishimune, Y., and Morita, T. (1998). The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol. Cell 1, 707-718.
48. Yu, R.N., Ito, M., Saunders, T.L., Camper, S.A., and Jameson, J.L. (1998). Role of Ahch in gonadal development and gametogenesis. Nat. Genet. 20, 353-356.
49. Yuan, L., Pelttari, J., Brundell, E., Björkroth, B., Zhao, J., Liu, J.-G., Brismar, H., Daneholt, B., and Höög, C. (1998). The synaptonemal complex protein SCP3 can form multistranded, cross-striated fibers in vivo. J. Cell Biol. 142, 331-339.
50. Zickler, D., and Kleckner, N. (1998). The leptotene-zygotene transition of meiosis. Annu. Rev. Genet. 32, 619-697.